MOLECULAR BIOLOGY OF DROSOPHILA LEARNING AND MEMORY

Summary

Principal Investigator: Ronald Davis
Affiliation: Texas Medical Center
Country: USA
Abstract: DESCRIPTION: The activity of many different types of molecules is modulated in the relevant neurons as an animal learns and stores information. Past research has focused on some of these types, such as molecules involved in second messenger metabolism, receptors, and some transcription factors. In Drosophila, the research has concentrated on molecules that are involved in cAMP-mediated signal transduction and that are expressed in mushroom body cells, neurons that appear to mediate olfactory learning in insects. These investigators are now turning their attention to molecules displayed at the surface of mushroom body cells, due to recent observations suggesting that a novel integrin and a surface member of the immunoglobulin superfamily of proteins are important for learning. A new learning mutant named volado, encodes an alpha-integrin expressed preferentially on mushroom body cells. In addition, products of the fasII gene, which encodes an NCAM-like molecule, are beautifully displayed on the axons of mushroom body cells and lesions of the gene produce deficits in olfactory classical conditioning. The proposed research will extend these observations to determine whether the deficits in conditioned behavior are general, or whether they are specific to olfactory classical conditioning. Conditional rescue experiments for both mutants are planned to help determine whether the lesions disrupt developmental processes that emerge as learning deficits, or whether the protein products are required physiologically during the process of learning. Candidates for the beta-integrin predicted to associate with the alpha-subunit will be evaluated for their roles in learning. Finally, genetic interaction studies are proposed to determine if these products are regulated by pathways of known importance; for example, the cAMP-mediated pathway, and whether there is an interaction between these two surface molecules. The investigators anticipate that the proposed research will reveal new insights and highlight the importance of cell surface molecules to the process of learning and memory. Furthermore, the identification of new molecules important for learning and memory will extend our knowledge, in general, of the molecular machinery underlying learning, and may provide insights into disease states that perturb cognitive processes.
Funding Period: 1987-12-01 - 2001-07-31
more information: NIH RePORT

Top Publications

  1. pmc Wnt signaling is required for long-term memory formation
    Ying Tan
    Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX 77030, USA
    Cell Rep 4:1082-9. 2013
  2. pmc Dopamine is required for learning and forgetting in Drosophila
    Jacob A Berry
    Department of Neuroscience, The Scripps Research Institute Florida, Jupiter, FL 33410, USA
    Neuron 74:530-42. 2012
  3. pmc Olfactory learning in Drosophila
    Germain U Busto
    Department of Neuroscience, The Scripps Research Institute Florida, Jupiter, Florida, USA
    Physiology (Bethesda) 25:338-46. 2010
  4. pmc The long-term memory trace formed in the Drosophila α/β mushroom body neurons is abolished in long-term memory mutants
    David Benjamin G Akalal
    Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, Texas 77030, USA
    J Neurosci 31:5643-7. 2011
  5. pmc Traces of Drosophila memory
    Ronald L Davis
    Department of Neuroscience, The Scripps Research Institute Florida, Jupiter, FL 33410, USA
    Neuron 70:8-19. 2011
  6. pmc A late-phase, long-term memory trace forms in the γ neurons of Drosophila mushroom bodies after olfactory classical conditioning
    David Benjamin G Akalal
    Department of Molecular and Cellular Biology and Menninger Department of Psychiatry and Behavioral Sciences, Baylor College of Medicine, Houston, Texas 77030, USA
    J Neurosci 30:16699-708. 2010
  7. pmc Gilgamesh is required for rutabaga-independent olfactory learning in Drosophila
    Ying Tan
    Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX 77030, USA
    Neuron 67:810-20. 2010
  8. pmc A distinct set of Drosophila brain neurons required for neurofibromatosis type 1-dependent learning and memory
    Monica E Buchanan
    Department of Molecular and Human Genetics and Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX 77030, USA
    J Neurosci 30:10135-43. 2010
  9. pmc A dual role for the adaptor protein DRK in Drosophila olfactory learning and memory
    Anastasios Moressis
    Institute of Molecular Biology and Genetics, Biomedical Sciences Research Centre Alexander Fleming, Vari 16672, Greece
    J Neurosci 29:2611-25. 2009
  10. pmc The GABAA receptor RDL suppresses the conditioned stimulus pathway for olfactory learning
    Xu Liu
    Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, Texas 77030, USA
    J Neurosci 29:1573-9. 2009

Scientific Experts

  • Ronald Davis
  • Ying Tan
  • David Benjamin G Akalal
  • Xu Liu
  • Dinghui Yu
  • Monica E Buchanan
  • Jacob A Berry
  • Isaac Cervantes-Sandoval
  • Germain U Busto
  • Anastasios Moressis
  • Katherine M Parisky
  • Louise Nicholson
  • Eric P Nicholas
  • Anke R Friedrich
  • Kyung An Han
  • Efthimios M C Skoulakis
  • Elias Pavlopoulos
  • Haig Keshishian
  • Elena Kuklin
  • Gunisha K Singh
  • James J L Hodge
  • Keongjin Kang
  • KyeongJin Kang
  • GREGG W ROMAN
  • Leslie C Griffith
  • Paul A Garrity
  • Michael Rosbash
  • Jose Agosto
  • Stefan R Pulver
  • Yuhua Shang
  • Thomas Osterwalder
  • William C Krause
  • Alex C Keene
  • Anjana Srivatsan
  • Scott Waddell

Detail Information

Publications18

  1. pmc Wnt signaling is required for long-term memory formation
    Ying Tan
    Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX 77030, USA
    Cell Rep 4:1082-9. 2013
    ..Thus, inhibiting three key components of the Wnt signaling pathway in adult mushroom bodies impairs LTM, indicating that this pathway mechanistically underlies this specific form of memory. ..
  2. pmc Dopamine is required for learning and forgetting in Drosophila
    Jacob A Berry
    Department of Neuroscience, The Scripps Research Institute Florida, Jupiter, FL 33410, USA
    Neuron 74:530-42. 2012
    ..We propose a dual role for dopamine: memory acquisition through dDA1 signaling and forgetting through DAMB signaling in the mushroom body neurons...
  3. pmc Olfactory learning in Drosophila
    Germain U Busto
    Department of Neuroscience, The Scripps Research Institute Florida, Jupiter, Florida, USA
    Physiology (Bethesda) 25:338-46. 2010
    ..The results from these and other experiments also indicate that cross talk between mushroom bodies and several other brain regions is critical for memory formation...
  4. pmc The long-term memory trace formed in the Drosophila α/β mushroom body neurons is abolished in long-term memory mutants
    David Benjamin G Akalal
    Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, Texas 77030, USA
    J Neurosci 31:5643-7. 2011
    ..These observations elevate the significance of this LTM trace given that 26 independent mutants all exhibit a defect in the trace, and further suggest that the calcium trace is a fundamental mechanism underlying Drosophila LTM...
  5. pmc Traces of Drosophila memory
    Ronald L Davis
    Department of Neuroscience, The Scripps Research Institute Florida, Jupiter, FL 33410, USA
    Neuron 70:8-19. 2011
    ....
  6. pmc A late-phase, long-term memory trace forms in the γ neurons of Drosophila mushroom bodies after olfactory classical conditioning
    David Benjamin G Akalal
    Department of Molecular and Cellular Biology and Menninger Department of Psychiatry and Behavioral Sciences, Baylor College of Medicine, Houston, Texas 77030, USA
    J Neurosci 30:16699-708. 2010
    ..These results demonstrate that behavioral long-term olfactory memory is encoded as modifications of calcium influx into distinct MB neurons during overlapping but different windows of time after training...
  7. pmc Gilgamesh is required for rutabaga-independent olfactory learning in Drosophila
    Ying Tan
    Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX 77030, USA
    Neuron 67:810-20. 2010
    ..Therefore, gish participates in a rutabaga-independent pathway for memory formation and accounts for some of the residual learning that occurs in rutabaga mutants...
  8. pmc A distinct set of Drosophila brain neurons required for neurofibromatosis type 1-dependent learning and memory
    Monica E Buchanan
    Department of Molecular and Human Genetics and Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX 77030, USA
    J Neurosci 30:10135-43. 2010
    ....
  9. pmc A dual role for the adaptor protein DRK in Drosophila olfactory learning and memory
    Anastasios Moressis
    Institute of Molecular Biology and Genetics, Biomedical Sciences Research Centre Alexander Fleming, Vari 16672, Greece
    J Neurosci 29:2611-25. 2009
    ....
  10. pmc The GABAA receptor RDL suppresses the conditioned stimulus pathway for olfactory learning
    Xu Liu
    Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, Texas 77030, USA
    J Neurosci 29:1573-9. 2009
    ..The combined data suggest that RDL suppresses olfactory learning via CS pathway involvement...
  11. pmc The GABAergic anterior paired lateral neuron suppresses and is suppressed by olfactory learning
    Xu Liu
    Department of Molecular and Cellular Biology, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
    Nat Neurosci 12:53-9. 2009
    ..These results demonstrate a mutual suppression between the GABAergic APL neuron and olfactory learning, and emphasize the functional neuroplasticity of the GABAergic system as a result of learning...
  12. pmc PDF cells are a GABA-responsive wake-promoting component of the Drosophila sleep circuit
    Katherine M Parisky
    Department of Biology, Brandeis University, Waltham, MA 02454 9110, USA
    Neuron 60:672-82. 2008
    ....
  13. pmc Spatial and temporal control of gene expression in Drosophila using the inducible GeneSwitch GAL4 system. I. Screen for larval nervous system drivers
    Louise Nicholson
    MCDB Department, Yale University, New Haven, CT 06520 8103, USA
    Genetics 178:215-34. 2008
    ..However, >90% of the neuron-specific driver lines showed little or no background activity, making them particularly useful for inducible expression studies...
  14. pmc GABAA receptor RDL inhibits Drosophila olfactory associative learning
    Xu Liu
    Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX 77030, USA
    Neuron 56:1090-102. 2007
    ..Together, these data suggest that RDL negatively modulates olfactory associative learning, possibly by gating the input of olfactory information into the MBs...
  15. pmc Drosophila alpha/beta mushroom body neurons form a branch-specific, long-term cellular memory trace after spaced olfactory conditioning
    Dinghui Yu
    Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, Texas 77030, USA
    Neuron 52:845-55. 2006
    ....
  16. pmc Roles for Drosophila mushroom body neurons in olfactory learning and memory
    David Benjamin G Akalal
    Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, Texas 77030, USA
    Learn Mem 13:659-68. 2006
    ....
  17. ncbi Drosophila DPM neurons form a delayed and branch-specific memory trace after olfactory classical conditioning
    Dinghui Yu
    Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, Texas 77030, USA
    Cell 123:945-57. 2005
    ..DPM neurons are therefore "odor generalists" and form a delayed, branch-specific, and amnesiac-dependent memory trace that may guide behavior after acquisition...
  18. ncbi Olfactory memory formation in Drosophila: from molecular to systems neuroscience
    Ronald L Davis
    Department of Molecular and Cellular Biology, Department of Psychiatry and Behavioral Sciences, Baylor College of Medicine, Houston, TX 77030, USA
    Annu Rev Neurosci 28:275-302. 2005
    ..Finally, the genes identified to participate in Drosophila olfactory learning have conserved roles in mammalian organisms, highlighting the value of Drosophila for gene discovery...